Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts

English version České info

Pathogens switching to new hosts can result in the emergence of new infectious diseases, and determining which species are likely to be sources of such host shifts is essential to understanding disease threats to both humans and wildlife. However, the factors that determine whether a pathogen can infect a novel host are poorly understood. We have examined the ability of three host-specific RNA-viruses (Drosophila sigma viruses from the family Rhabdoviridae) to persist and replicate in 51 different species of Drosophilidae. Using a novel analytical approach we found that the host phylogeny could explain most of the variation in viral replication and persistence between different host species. This effect is partly driven by viruses reaching a higher titre in those novel hosts most closely related to the original host. However, there is also a strong effect of host phylogeny that is independent of the distance from the original host, with viral titres being similar in groups of related hosts. Most of this effect could be explained by variation in general susceptibility to all three sigma viruses, as there is a strong phylogenetic correlation in the titres of the three viruses. These results suggest that the source of new emerging diseases may often be predictable from the host phylogeny, but that the effect may be more complex than simply causing most host shifts to occur between closely related hosts.

Vyšlo v časopise: Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002260
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002260

Souhrn

Zdroje

1. HahnBHShawGMDe CockKMSharpPM 2000 AIDS -⁠ AIDS as a zoonosis: Scientific and public health implications. Science 287 607 614

2. WebbyRJWebsterRG 2001 Emergence of influenza A viruses. Philos Trans R Soc Lond B Biol Sci 356 1817 1828

3. LiuWMLiYYLearnGHRudicellRSRobertsonJD 2010 Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467 420-U467

4. LeroyEMRouquetPFormentyPSouquiereSKilbourneA 2004 Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303 387 390

5. Roelke-parkerMEMunsonLPackerCKockRCleavelandS 1996 A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379 441 445

6. WoolhouseMEHaydonDTAntiaR 2005 Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20 238 244

7. JonesKEPatelNGLevyMAStoreygardABalkD 2008 Global trends in emerging infectious diseases. Nature 451 990 993

8. LipsKRBremFBrenesRReeveJDAlfordRA 2006 Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A 103 3165 3170

9. VasilakisNWeaverSC 2008 The history and evolution of human dengue emergence. Adv Virus Res 72 1 76

10. LanciottiRSRoehrigJTDeubelVSmithJParkerM 1999 Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286 2333 2337

11. EngelstadterJHurstGD 2006 The dynamics of parasite incidence across host species. Evol Ecol 20 603 616

12. RussellJAGoldman-HuertasBMoreauCSBaldoLStahlhutJK 2009 Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63 624 640

13. TurnerPEElenaSF 2000 Cost of host radiation in an RNA virus. Genetics 156 1465 1470

14. DuffySBurchCLTurnerPE 2007 Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61 2614 2622

15. ThompsonJN 1994 The Coevolutionary Process. Chicago The University of Chicago press 1 376

16. DaviesTJPedersenAB 2008 Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc Biol Sci 275 1695 1701

17. de VienneDMHoodMEGiraudT 2009 Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol 22 2532 2541

18. GilbertGSWebbCO 2007 Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci U S A 104 4979 4983

19. PerlmanSJJaenikeJ 2003 Infection success in novel hosts: An experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution 57 544 557

20. TinsleyMCMajerusMEN 2007 Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts. BMC Evol Biol 7 238

21. WoolhouseMEGowtage-SequeriaS 2005 Host range and emerging and reemerging pathogens. Emerg Infect Dis 11 1842 1847

22. ParrishCRHolmesECMorensDMParkECBurkeDS 2008 Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72 457 470

23. BaranowskiERuiz-JaraboCMDomingoE 2001 Evolution of cell recognition by viruses. Science 292 1102 1105

24. WoolhouseME 2002 Population biology of emerging and re-emerging pathogens. Trends Microbiol 10 S3 7

25. KuikenTHolmesECMcCauleyJRimmelzwaanGFWilliamsCS 2006 Host species barriers to influenza virus infections. Science 312 394 397

26. HavardSEslinPPrevostGDouryG 2009 Encapsulation ability: Are all Drosophila species equally armed? An investigation in the obscura group. Can J Zoo 87 635 641

27. StreickerDGTurmelleASVonhofMJKuzminIVMcCrackenGF 2010 Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats. Science 329 676 679

28. CharlestonMARobertsonDL 2002 Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51 528 535

29. LongdonBObbardDJJigginsFM 2010 Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. Proc Biol Sci 277 35 44

30. LongdonBWilfertLOsei-PokuJCagneyHObbardDJ 2011 Host switching by a vertically-transmitted rhabdovirus in Drosophila. Biol Lett. E-pub ahead of print doi:10.1098/rsbl.2011.0160

31. BrunGPlusN 1980 The viruses of Drosophila. AshburnerMWrightTRF The genetics and biology of Drosophila New York Academic Press 625 702

32. LongdonBWilfertLObbardDJJigginsFM 2011 Rhabdoviruses in two species of Drosophila: vertical transmission and a recent sweep. Genetics. E-pub ahead of print doi:10.1534/genetics.111.127696

33. JoussetFX 1969 Preliminary Studies of Drosophila Sigma-Virus Proliferation in Taxonomically Different Insects. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie D 269 1035

34. WilfertLJigginsFM 2010 Host-parasite coevolution: genetic variation in a virus population and the interaction with a host gene. J Evol Biol 23 1447 1455

35. SullivanWAshburnerMHawleyS 2000 Drosophila Protocols. New York Cold Spring Harbor Laboratory Press 655 660

36. BianGXuYLuPXieYXiZ 2010 The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6 e1000833

37. HedgesLMBrownlieJCO'NeillSLJohnsonKN 2008 Wolbachia and Virus Protection in Insects. Science 322 702 702

38. MoreiraLAIturbe-OrmaetxeIJefferyJALuGPykeAT 2009 A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139 1268 1278

39. TeixeiraLFerreiraAAshburnerM 2008 The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster. Plos Biol 6 2753 2763

40. ZhouWRoussetFO'NeilS 1998 Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265 509 515

41. HueyRBMoreteauBMoreteauJCGibertPGilchristGW 2006 Sexual size dimorphism in a Drosophila clade, the D.obscura group. Zoology 109 318 330

42. SokoloffA 1966 Morphological Variation in Natural and Experimental Populations of Drosophila Pseudoobscura and Drosophila Persimilis. Evolution 20 49 71

43. GilchristGWHueyRBSerraL 2001 Rapid evolution of wing size clines in Drosophila subobscura. Genetica 112-113 273 286

44. RasbandWS 1997 ImageJ, Version 1.43u. U. S. National Institutes of Health, Bethesda, Maryland, USA. Available: http://imagej.nih.gov/ij/

45. DrummondAJRambautA 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 214

46. ShapiroBRambautADrummondAJ 2006 Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23 7 9

47. RambautADrummondAJ 2007 Tracer v1.4, Available: http://beast.bio.ed.ac.uk/Tracer

48. RambautA 2006 FigTree. v1.3. Available: http://tree.bio.ed.ac.uk/software/figtree/

49. HadfieldJDNakagawaS 2010 General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23 494 508

50. HousworthEAMartinsEPLynchM 2004 The phylogenetic mixed model. Am Nat 163 84 96

51. LynchM 1991 Methods For The Analysis Of Comparative Data In Evolutionary Biology. Evolution 45 1065 1080

52. MartinsEPDiniz-FilhoJAHousworthEA 2002 Adaptive constraints and the phylogenetic comparative method: a computer simulation test. Evolution 56 1 13

53. HadfieldJD 2010 MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. J Stat Software 33 1 22

54. GilmourAGogelBCullisBWElhamSThompsonR 2002 ASReml User Guide Release 1.0.

55. van der LindeKHouleDSpicerGSSteppanSJ 2010 A supermatrix-based molecular phylogeny of the family Drosophilidae. Genetics Res 92 25 38

56. O'GradyPDesalleR 2008 Out of Hawaii: the origin and biogeography of the genus Scaptomyza (Diptera: Drosophilidae). Biol Lett 4 195 199

57. WilsonAJ 2008 Why h(2) does not always equal V-A/V-P? J of Evol Biol 21 647 650

58. PagelM 1999 Inferring the historical patterns of biological evolution. Nature 401 877 884

59. FreckletonRPHarveyPHPagelM 2002 Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160 712 726

60. RussoCATakezakiNNeiM 1995 Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12 391 404

61. PagelM 1994 Detecting Correlated Evolution On Phylogenies -⁠ A General-Method For The Comparative-Analysis Of Discrete Characters. Proc Biol Sci 255 37 45

62. BreglianoJC 1970 Study of Infection of Germ Line in Female Drosophila Infected with Sigma Virus .2. Evidence of a Correspondance between Ovarian Cysts with Increased Virus Yield and Stabilized Progeny. Annales De L Institut Pasteur 119 685 704

63. L'HeritierP 1957 The hereditary virus of Drosophila. Adv Virus Res 5 195 245

64. JensenKHLittleTJSkorpingAEbertD 2006 Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4 e197

65. HullR 2009 Comparative plant virology. London Elsevier Academic Press 39 40

66. BaerGMShaddockJHQuirionRDamTVLentzTL 1990 Rabies susceptibility and acetylcholine receptor. Lancet 335 664 665

67. ObbardDJJigginsFMBradshawNJLittleTJ 2011 Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol Biol Evol 28 1043 1056

68. ObbardDJJigginsFMHalliganDLLittleTJ 2006 Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16 580 585

69. ObbardDJWelchJJKimKWJigginsFM 2009 Quantifying adaptive evolution in the Drosophila immune system. PLoS Genet 5 e1000698

70. KolaczkowskiBHupaloDNKernAD 2011 Recurrent adaptation in RNA interference genes across the Drosophila phylogeny. Mol Biol Evol 28 1033 1042

71. JigginsFMKimKW 2005 The evolution of antifungal peptides in Drosophila. Genetics 171 1847 1859

72. SacktonTBLazzaroBPSchlenkeTAEvansJDHultmarkD 2007 Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39 1461 1468

73. ObbardDJGordonKHBuckAHJigginsFM 2009 The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci 364 99 115

74. HainDBettencourtBROkamuraKCsorbaTMeyerW 2010 Natural variation of the amino-terminal glutamine-rich domain in Drosophila argonaute2 is not associated with developmental defects. Plos One 5 e15264

75. RossmannMGTaoY 1999 Structural insight into insect viruses. Nat Struct Biol 6 717 719

76. KooninEVWolfYINagasakiKDoljaVV 2008 The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6 925 939

77. WalkerPJKongsuwanK 1999 Deduced structural model for animal rhabdovirus glycoproteins. J Gen Virol 80 1211 1220

78. FuZF 2005 Genetic comparison of the rhabdoviruses from animals and plants. World of Rhabdoviruses. Curr topics Microbiol and Imm 292 1 24

79. FelsensteinJ 1985 Phylogenies and the Comparative Method. Am Nat 125 1 15